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Evolution andNatural History of the CottonGenus
Jonathan F. Wendel, Curt Brubaker, Ines Alvarez, Richard Cronn,
and James McD. Stewart
Abstract We present an overview of the evolution and diversity in Gossypium
(the cotton genus). This framework facilitates insight into fundamental aspects
of plant biology, provides the necessary underpinnings for effective utilization
of cotton genetic resources, and guides exploration of the genomic basis of
morphological diversity in the genus. More than 50 species of Gossypium are
distributed in arid to semi-arid regions of the tropics and subtropics. Included
are four species that independently have been domesticated for their fiber, two
each in Africa-Asia and the Americas. Gossypium species exhibit extraordin-
ary morphological variation, ranging from trailing herbaceous perennials to
!15 m trees with a diverse array of reproductive and vegetative characteris-
tics. A parallel level of cytogenetic and genomic diversity has arisen during the
global radiation of the genus, leading to the evolution of eight groups of diploid
(n¼ 13) species (genome groups A through G, and K). Data implicate an origin
for Gossypium about 5–10 million years ago and a rapid early diversification of
the major genome groups. Allopolyploid cottons appear to have arisen within
the last 1–2 million years, as a consequence of trans-oceanic dispersal of an
A-genome taxon to the NewWorld followed by hybridization with an indigen-
ous D-genome diploid. Subsequent to formation, allopolyploids radiated into
three modern lineages, two of which contain the commercially important species
G. hirsutum and G. barbadense.
1 Introduction to Gossypium diversity
Because the cotton genus (Gossypium L.) is so important to economies around
the world, it has long attracted the attention of agricultural scientists, taxono-
mists, and evolutionary biologists. Accordingly, and notwithstanding the
J.F. Wendel (*)
Department of Ecology, Evolution, and Organismal Biology, Iowa State University,
Ames, Iowa 50011
e-mail: jfw@iastate.edu
A.H. Paterson (ed.), Genetics and Genomics of Cotton,
Plant Genetics and Genomics: Crops and Models 3,
DOI 10.1007/978-0-387-70810-2_1, ! Springer ScienceþBusiness Media, LLC 2009
3
remaining gaps in our knowledge, a great deal is understood about the origin
and diversification of the genus. Especially in the last two decades, modern
molecular technologies have been brought to bear on such classic questions as
the origin of the polyploid species, the relationships among species and species
groups, and the origins of the domesticated forms from their wild progenitors.
Perhaps the most striking aspect of this history is that it is so widespread in
scope, involving ancient human cultures on several continents and a convergent
or parallel plant domestication process from divergent and geographically
isolated wild ancestors. This parallel domestication process involved four species,
two from the Americas, G. hirsutum and G. barbadense, and two from Africa-
Asia, G. arboreum and G. herbaceum. In each of these four cases, aboriginal
peoples discovered thousands of years ago that the unique properties of cotton
fibers made them useful for ropes, textiles and other applications. Each of the
domesticated species has its own unique history of domestication, diversifica-
tion, and utilization, as detailed in many papers describing various stages in the
domestication process, the origin of present patterns of genetic diversity, the
shape and severity of genetic bottlenecks that accompanied the development of
landraces and cultivars, and the influence of recent human history on geographic
patterns of cultivation (Brubaker, Bourland and Wendel 1999; Brubaker and
Wendel 1994, 2001; Hutchinson 1951, 1954, 1959; Hutchinson, Silow and Ste-
phens 1947; Percy and Wendel 1990; Wendel, Brubaker and Percival 1992;
Wendel, Olson and Stewart 1989).
This rich history involved human shaping and molding of naturally occur-
ring diversity that originated through the process of evolutionary diversifica-
tion over a period of millions of years, a legacy we continue to exploit today
through deliberate introgression of alien germplasm from diverse, wild gene
pools. Given current threats to global ecosystems, it has never been more
critical than it is today to recognize this legacy of speciation and diversification.
Toward this end a synopsis of the present understanding of the evolutionary
history and taxonomy ofGossypium is given, and in the process an entry into the
relevant body of literature is provided for the serious reader.
2 Origin of the Genus Gossypium
The cotton genus belongs to a small taxonomic tribe, the Gossypieae, that
includes only eight genera (Fryxell 1968; Fryxell 1979). Four of these genera
are small with restricted geographic distributions (Fryxell 1968; Fryxell 1979)
including Lebronnecia (Marquesas Islands),Cephalohibiscus (NewGuinea, Solo-
mon Islands), Gossypioides (east Africa, Madagascar), and Kokia (Hawaii). The
tribe also includes four moderately sized genera with broader geographic ranges:
Hampea, with 21 neotropical species; Cienfuegosia, a diverse genus with 25
species from the neotropics and parts of Africa; Thespesia, with 17 tropical
species; and last but not least,Gossypium, the largest and most widely distributed
4 J.F. Wendel et al.
genus in the tribe with more than 50 species (Fryxell 1992; Stewart, Craven,
Brubaker and Wendel 2008; Stewart and Ulloa unpublished).
Molecular phylogenetic analyses have clarified several aspects of the evolu-
tionary history of the tribe (Cronn, Small, Haselkorn and Wendel 2002;
Seelanan, Schnabel and Wendel 1997). Most important has been the demon-
stration that the group of species recognized as belonging to Gossypium do in
fact constitute a single natural lineage, despite their global distribution and
extraordinary morphological and cytogenetic diversity. A second discovery
has been the identity of the closest relatives of Gossypium, i.e., the African-
Madagascan genusGossypioides and the Hawaiian endemic genusKokia. These
latter genera may thus be used as phylogenetic outgroups for studying evolu-
tionary patterns and processes within Gossypium. A third insight concerns the
temporal component to the genealogy, which is evident in sequence divergence
data that serve as a proxy for time. Using this ‘‘molecular clock’’, Seelanan,
Schnabel and Wendel (1997) suggested that Gossypium branched off from
Kokia and Gossypioides approximately 12.5 million years ago (mya), in agree-
ment with a later, more extensive data set based on 10 different nuclear genes
(Cronn, Small, Haselkorn andWendel 2002). Thus,Gossypium appears to have
diverged from its closest relatives during the Miocene, perhaps 10–15 mya,
subsequently spreading around the world via trans-oceanic dispersal to acquire
its modern geographic range.
3 Diversification and Speciation of the Diploid Cotton Species
From its origin millions of years ago, Gossypium underwent speciation and
diversification, achieving a nearly worldwide distribution with several pri-
mary centers of diversity in the arid or seasonally arid tropics and subtropics
(Table 1). Species-rich regions include Australia, especially the Kimberley
region in NW Australia, the Horn of Africa and southern Arabian Peninsula,
and the western part of central and southern Mexico. Recognition of these
groups of related species and their individual constituents reflects accu-
mulated scientific understanding that emerged from basic plant exploration
and taxonomic and evolutionary study. The taxonomy of the genus has been
well-studied (Cronn, Small, Haselkorn and Wendel 2002; Fryxell 1979, 1992;
Hutchinson, Silow and Stephens 1947; Saunders 1961; Seelanan, Schnabel and
Wendel 1997; Watt 1907), with the most modern and widely followed taxo-
nomic treatments being those of Fryxell (1979; 1992) inwhich species are grouped
into four subgenera and eight sections (Table 1). This classification system is
based primarilyon morphological and geographical evidence, although most
infra-generic alignments are congruent with cytogenetic and molecular data
sets as well (see Chapter 11 by Mergeai, this volume).
At present, Gossypium includes approximately 50 species (Fryxell 1992), but
remarkably, new species continue to be discovered (Fryxell 1992; Stewart,
Craven, Brubaker and Wendel 2008; Ulloa, Stewart, Garcia, Godoy, Gaytán
Evolution and Natural History of the Cotton Genus 5
Table 1 Diversity and geographic distribution of the major lineages of Gossypium. Genomic
placements of species enclosed by parentheses are yet to be determined
Genome
group
Number of
species
Recognized
species Geographic distribution
A 2 G. arboreum,
G. herbaceum
Africa, Asia
B 3 (4) G. anomalum
G. triphyllum
G. capitis-viridis
(G. trifurcatum)
Africa, Cape Verde Islands
C 2 G. sturtianum
G. robinsonii
Australia
D 13(14) G. thurberi
G. armourianum
G. harknessii
G. davidsonii
G. klotschianum
G. aridum
G. raimondii
G. gossypioides
G. lobatum
G. trilobatum
G. laxum
G. turneri
G. schwendimanii
(G. sp.nov.)
Primarily Mexico; also Peru, Galapagos
Islands, Arizona
E 5 (9) G. stocksii
G. somalense
G. areysianum
G. incanum
G. trifurcatum
(G. benidirense)
(G. bricchettii)
(G. vollesenii)
(G. trifurcatum)
Arabian Penisula, Northeast Africa,
Southwest Asia
F 1 G. longicalyx East Africa
G 3 G. bickii
G. australe
G. nelsonii
Australia
K 12 G. anapoides
G. costulatum
G. cunninghamii
G. enthyle
G. exiguum
G. londonderriense
G. marchantii
G. nobile
G. pilosum
G. populifolium
G. pulchellum
G. rotundifolium
NW Australia, Cobourg Peninsula, NT
6 J.F. Wendel et al.
and Acosta 2006). The genus is extraordinarily diverse; species morphologies
range from fire-adapted, herbaceous perennials in NWAustralia to trees in SW
Mexico that escape the dry season by dropping their leaves. Corolla colors span
a rainbow of blue to purple (G. triphyllum), mauves and pinks (‘‘Sturt’s Desert
Rose’’, G. sturtianum, is the official floral emblem of the Northern Territory,
Australia), whites and pale yellows (NWAustralia,Mexico, Africa-Arabia) and
even a deep sulphur-yellow (G. tomentosum fromHawaii). Seed coverings range
from nearly glabrous to the naked eye (e.g.,G. klotzschianum andG. davidsonii),
to short stiff, dense, brown hairs that aid in wind-dispersal (G. australe,
G. nelsonii), to the long, fine white fibers that characterize highly improved
forms of the four cultivated species. There are even seeds that produce fat
bodies to facilitate ant-dispersal (Seelanan, Brubaker, Stewart, Craven and
Wendel 1999).
As the genus diversified and spread, it underwent extensive chromosomal
evolution (see Chapter 11 by Konan et al. and Chapter 11 by Mergeai, this
volume). Although all diploid species share the same chromosome number
(n ¼ 13), there is more than three-fold variation in DNA content per genome
(Hendrix and Stewart 2005). Chromosome morphology is similar among
closely related species, and this is reflected in the ability of related species to
form hybrids that display normal meiotic pairing and sometimes high F1
fertility. In contrast, crosses among more distant relatives may be very difficult
to effect, and those that are successful are characterized by meiotic abnormal-
ities. The collective observations of pairing behavior, chromosome sizes, and
relative fertility in interspecific hybrids led to the designation of single-letter
genome symbols (Beasley 1941) for related clusters of species. Presently, eight
diploid genome groups (A through G, plus K) are recognized (Endrizzi,
Turcotte and Kohel 1985; Stewart 1995). This cytogenetic partition of the
genus is largely congruent with taxonomic and phylogenetic divisions. A brief
introduction to the major groups of diploid cotton species follows.
3.1 Australian Species
Australian cottons (subgenus Sturtia) comprise 16 named species as well as a
new species whose description is in press (Stewart, Craven, Brubaker and
Table 1 (continued)
Genome
group
Number of
species
Recognized
species Geographic distribution
AD 5 G. hirsutum
G. barbadense
G. tomentosum
G. mustelinum
G. darwinii
New World tropics and subtropics,
including Hawaii
Evolution and Natural History of the Cotton Genus 7
Wendel 2008). Collectively, these taxa comprise the C-, G-, and K-genome
groups, with two, three, and twelve species, respectively. These three groups
of species are implicated by DNA sequence data (Liu, Brubaker, Green,
Marshall, Sharp and Singh 2001; Seelanan, Brubaker, Stewart, Craven and
Wendel 1999; Seelanan, Schnabel and Wendel 1997) to be natural lineages,
consistent with their formal alignments into the taxonomic sections Sturtia
(C-genome), Hibiscoidea (G-genome), and Grandicalyx (K-genome). Relation-
ships among the three groups, however, remain unclear. Some data place
G. robinsonii as basal within the entire assemblage ofAustralian species (DeJoode
andWendel 1992), suggesting that radiation ofGossypium inAustralia proceeded
eastward from the westernmost portion of the continent. Whether this basal
position will withstand the scrutiny of other data sets is an open question, as
the most recent analyses (Liu, Brubaker, Mergeai, Cronn and Wendel 2001;
Seelanan, Brubaker, Stewart, Craven and Wendel 1999; Seelanan, Schnabel
and Wendel 1997) are equivocal in this regard.
With respect to the taxonomy within each of the three Australian genome
groups, there is little uncertainty for the C- and G-genome groups, as these are
well represented in collections and have been thoroughly studied (DeJoode and
Wendel 1992; Fryxell 1979, 1992; Liu, Brubaker, Mergeai, Cronn and Wendel
2001; Seelanan, Brubaker, Stewart, Craven andWendel 1999; Seelanan, Schnabel
and Wendel 1997; Wendel, Stewart and Rettig 1991). Much less certain is the
taxonomy of the K-genome species, which are all placed in sectionGrandicalyx.
Collecting expeditions to the Kimberley area have enhanced our understanding
of diversity within the group and have resulted in the discovery of at least seven
new species (Fryxell, Craven and Stewart 1992; Stewart, Craven, Brubaker and
Wendel, 2008). These unusual species have a distinctive geography, morphol-
ogy and ecology, and exhibit a syndrome of features that are characteristic of
fire-adaptation. In particular, they are herbaceous perennials with a bi-seasonal
growth pattern whereby vegetative growth dies back during the dry season to
underground rootstocks that initiate a new cycle of growth with the onset of the
next wet season or following a fire. Species in sectionGrandicalyx have flowers
that are upright when open but that become pendant following pollination so
that at maturity, the capsules release sparsely haired, ant-dispersed seeds that
bear elaiosomes (fat bodies) to aid in attracting ants. Many of these species are
poorly represented in collections and not well understood taxonomically.
Molecular phylogenetic analyses have yielded conflicting results regarding
interspecific relationships in this group (Liu, Brubaker, Mergeai, Cronn and
Wendel 2001; Seelanan, Brubaker, Stewart, Craven and Wendel 1999).
3.2 African-Asian Species
Fourteen species from Africa and Arabia are recognized in the most recent
taxonomic treatment of the genus (Fryxell 1992), collectively in subgenus
8 J.F. Wendel et al.
Gossypium. The taxonomic section Gossypium contains four subsections,
whereas section Serrata contains only G. trifurcatum from the desert area of
eastern Somalia. The presence of dentate leaves raised the possibility that it
may not belong in Gossypium, but recent molecular work clearly established
this poorly known entity as a bona fide if unusual cotton species (Rapp, Alvarez
and Wendel 2005). This latter example underscores the provisional nature of
much of the taxonomy of the African-Arabian species of Gossypium, which are
sorely in need of basic plant exploration and systematic study. Within section
Pseudopambak, species recognition and definition are in some cases based on
limited herbariummaterial (e.g., G. benadirense, G. bricchettii, G. vollesenii) and
seeds have not been collected. Consequently, no analyses have been conducted on
cytogenetic characteristics nor molecular phylogenetic affinities.
From a cytogenetic standpoint, the African-Arabian species exhibit consid-
erable diversity, collectively accounting for four of the eight genome groups (A-,
B-, E-, and F-). The A-genome group comprises the two cultivated cottons of
subsection Gossypium, G. arboreum and G. herbaceum. Three African species in
subsectionAnomala (G. anomalum, G. captis-viridis andG. triphyllum) comprise
the B genome.Gossypium trifurcatummay also belong to the B genome, but this
has not been established. The sole F-genome species, G. longicalyx, is cytogen-
etically distinct (Phillips 1966), morphologically isolated (Fryxell 1971; Fryxell
1992) and, according to Fryxell (1979), is perhaps adapted to more mesic
conditions than any other diploid Gossypium species. The remaining African-
Asian species, those of subsection Pseudopambak, are considered to possess
E-genomes, although this has yet to be verified.
3.3 American Diploid Species
SubgenusHouzingenia contains two sections and six subsections, whose species
collectively represent the New World D-genome diploids. These species have
been more thoroughly studied than most, and consequently their taxonomy is
reasonably well-understood. This subgenus has also received considerable phy-
logenetic attention (Álvarez, Cronn and Wendel 2005; Cronn, Small, Haselk-
orn and Wendel 2002; Cronn, Small, Haselkorn and Wendel 2003; Small and
Wendel 2005; Wendel and Albert 1992), which provides support for the natur-
alness of most of the subsections. Evolutionary relationships among the appar-
ently natural subsections are less certain, however (Álvarez, Cronn andWendel
2005), although available evidence suggests that G. gossypioides is basal-most
within the subgenus (Cronn, Small, Haselkorn and Wendel 2003).
Twelve of the 14 D-genome diploid species are endemic to western Mexico,
thus this area is the center of diversity of the D genome. Likely, the lineage
became established and initially diversified in this region. Later range exten-
sions are inferred to have arisen from relatively recent (probably Pleistocene)
long-distance dispersals, leading to the evolution of endemics in Peru
(G. raimondii) and the Galapagos Islands (G. klotzschianum).
Evolution and Natural History of the Cotton Genus 9
4 Origin and Diversification of the Polyploid Cottons
Classic cytogenetic investigations demonstrated that the American tetraploid
species are allopolyploids containing two resident genomes, an A-genome from
Africa or Asia, and aD-genome similar to those found in the American diploids
(Beasley 1940; Denham 1924; Harland 1940; Skovsted 1934, 1937; Webber,
1935). Additional support for the hypothesis of an allopolyploid origin of the
American tetraploids emerged in subsequent decades from numerous sources
of evidence, including the synthesis of additional experimental allotetraploids
(Stewart 1995). This history and evidence is detailed in Endrizzi, Turcotte
and Kohel (1985), Wendel and Cronn (2003) and Chapter 11 by Mergeai, this
volume.
When did allopolyploid cottons first form, and how did this happen given
that the two diploid genomes involved (A and D) presently exist in species from
different hemispheres? This question was a classic botanical mystery for over
half a century (see Endrizzi, Turcotte and Kohel 1985), a mystery at least
partially solved through the recent use of molecular technologies. With respect
to the first part of the question, that of ‘‘when’’, gene sequence data convincingly
demonstrate that allopolyploid Gossypium originated prior to the evolution of
modern humans but relatively recently in geological terms, perhaps 1–2 mya, or
in the mid-Pleistocene (Cronn, Small, Haselkorn and Wendel 2002; Seelanan,
Schnabel and Wendel 1997; Senchina, Alvarez, Cronn, Liu, Rong, Noyes,
Paterson, Wing, Wilkins and Wendel 2003). With respect to the second part
of the question, that of polyploid parentage, it is now clear that both extant
A-genome species (G. arboreum, G. herbaceum) are equally divergent from the
A-genome of allopolyploid cottons and that the closest living relative of the
progenitor D-genome donor is G. raimondii (Endrizzi, Turcotte and Kohel
1985; Wendel and Cronn 2003). One aspect of the history of the polyploid
cottons that has become clear is that they all contain an A-genome cytoplasm,
andmost likely from a single source (Galau andWilkins 1989; Small andWendel
1999; Wendel 1989). Studies using nuclear (bi-parentally inherited) genes lead to
the same conclusion.Hence, evidence indicates that natural allopolyploid cottons
all derive from a single lineage.
Given a Pleistocene origin for allopolyploid cotton species, one may infer
that their morphological diversification and spread must have been relatively
rapid following polyploidization. At present, five allopolyploid species are
recognized. Gossypium darwinii is native to the Galapagos Islands, where it
may form large and continuous populations in some areas (Percy and Wendel
1990). Gossypium tomentosum, from the Hawaiian Islands, has a more diffuse
population structure, occurring mostly as scattered individuals and small
populations on several islands (DeJoode and Wendel 1992). A third allopoly-
ploid, G. mustelinum, is an uncommon species restricted to a relatively small
region of northeast Brazil (Wendel, Rowley and Stewart 1994). In addition to
these three truly wild species, there are two cultivated species (G. barbadense and
10 J.F. Wendel et al.
G. hirsutum), each of which has a large indigenous range, collectively encom-
passing a wealth of morphological forms that span the wild-to-domesticated
continuum (Brubaker and Wendel 1993, 1994, 2001; Fryxell 1979; Hutchinson
1951; Percy and Wendel 1990). Gossypium hirsutum is widely distributed in
Central and northern South America, the Caribbean, and even reaches distant
islands in the Pacific (Solomon Islands, Marquesas). Gossypium hirsutum is
thought to have a more northerly distribution than G. barbadense, with wild
populations occurring as far north (27838’N) as Tampa Bay (Stewart, personal
observation). However, recently Stewart and Bertoni (2007 unpublished) col-
lected a wild population of G. hirsutum in the Chaco state of Presidente Hayes,
Paraguay (!228S). Gossypium barbadense has a more southerly indigenous
range, centered in the northern third of South America but with a large region
of range overlap with G. hirsutum in the Caribbean.
Consideration of the distribution of the allopolyploid species suggests that
polyploidy led to the invasion of a new ecological niche. Fryxell (1965, 1979)
noted that in contrast to the majority of diploid species, allopolyploid species
typically occur in coastal habitats, at least those forms that arguably are truly
wild. Two species, both island endemics (G. darwinii and G. tomentosum), are
restricted to near coastlines, and for two others (G. barbadense andG. hirsutum),
wild forms occur in littoral habitats ringing the Gulf of Mexico, northwest
South America, and even on distant Pacific Islands. Fryxell (1965, 1979)
speculated that following initial formation, adaptation of the newly evolved
allopolyploid to littoral habitats enabled it to exploit the fluctuating sea levels
that characterized the Pleistocene. This ecological innovation is envisioned to
have facilitated initial establishment of the new polyploid lineage, and also may
have provided a means for the rapid dispersal of the salt-water tolerant seeds.
The recent discovery of G. hirsutum in Paraguay does not negate this hypoth-
esis, in that the population was located next to an area of seasonal water
accumulation suspected of being saline due to the many years of water accu-
mulation followed by evaporation. The timing and source of the initial intro-
duction of cotton to this area are unknown, but could involve bird dispersal.5 Phylogenetic Relationships in the Genus
A genealogical framework for the genus has been provided bymultiplemolecular
phylogenetic investigations (reviewed inWendel and Cronn 2003). Each of these
studies shows that genealogical lineages of species are congruent with genome
designations and geographical distributions. Cytogenetic studies (reviewed in
Chapter 11, this volume) further support this conclusion. Accordingly, each
genome group corresponds to a single natural lineage, and in most cases, these
lineages are also geographically cohesive. This information is summarized in a
depiction of our present understanding of relationships (Fig. 1).
Evolution and Natural History of the Cotton Genus 11
Several aspects of the phylogenetic history of Gossypium bear highlighting.
First, there exist four major lineages of diploid species corresponding to three
continents: Australia (C-, G-, K-genomes), the Americas (D-genome), and
Africa/Arabia (two lineages: one comprising the A-, B-, and F-genomes, and a
second containing the E-genome species). Second, the earliest divergence event
in the genus separated the New World D-genome lineage from the ancestor of
all OldWorld taxa. Thus, NewWorld and OldWorld diploids are phylogenetic
sister groups. Following this basal-most split in the genus, cottons comprising
the OldWorld lineage divided into three groups, namely, the Australian cottons
Fig. 1 Evolutionary history of Gossypium, as inferred from multiple molecular phylogenetic
data sets. The closest relative of Gossypium is a lineage containing the African-Madagascan
genus Gossypioides and the Hawaiian endemic genus Kokia. Following its likely origin 5–10
mya, Gossypium split into three major diploid lineages: the New World clade (D-genome);
the African-Asian clade (A-, B-, E- and F-genomes); and the Australian clade (C-, G-, and
K-genomes). This global radiation involved several trans-oceanic dispersal events and was
accompanied by morphological, ecological, and chromosomal differentiation (2C genome
sizes shown in white ellipses). Interspecific hybridization is implicated in the evolution of
approximately one-fourth of the genus. Allopolyploid cottons formed following trans-oceanic
dispersal of an A-genome diploid to the Americas, where the new immigrant underwent
hybridization, as female, with a native D-genome diploid similar to modern G. raimondii.
Polyploid cotton probably originated during the Pleistocene (1–2 mya), with the five modern
species representing the descendants of an early and rapid colonization of the New World
tropics and subtropics (See Color Insert)
12 J.F. Wendel et al.
(C-, G-, and K-genome species), the African-Arabian E-genome species, and
the African A-, B-, and F-genome cottons. Third, the African F-genome clade,
which consists of the sole speciesG. longicalyx, is definitively diagnosed as sister
to the A-genome species. This identifies the wild forms most closely related to
those first domesticated in the A-genome species G. arboreum and G. herba-
ceum. Because this relationship is revealed, prospects are raised for ultimately
understanding the genetic basis of the origin of useful, long lint. Fourth, the
major lineages of Gossypium were established in relatively rapid succession
shortly after the genus originated and diverged from the Kokia-Gossypioides
clade. The evolutionary picture thus envisioned is that there was a rapid and
global radiation early in the history of the genus, with temporally closely spaced
divergence events.
Allopolyploid cottons, including the two species of great commercial impor-
tance today (G. hirsutum and G. barbadense) are implicated to have formed
following a biological reunion of two genomes (A and D) that descended from
the earliest split in the genus. That is, the two constituent genomes of allopoly-
ploid cotton evolved first in different hemispheres and diverged for millions of
years, in isolation from one another. Allopolyploid cottons thus contain dupli-
cated but slightly divergent copies of most genes. Senchina et al. (2003) studied
48 pairs of these duplicates, and showed that on average, there is about 3–4%
sequence divergence between copies, although there is considerable variation
about this mean.
Consideration of the phylogeny of Fig. 1 in a temporal context and in light
of plate tectonic history leads to an inference of multiple intercontinental
dispersal events and other episodes of trans-oceanic travel during the evolu-
tionary history of the Gossypium. These include at least one dispersal between
Australia and Africa, another to the Americas (probablyMexico) leading to the
evolution of the D-genome diploids, and a second, much later colonization of
the New World by the A-genome ancestor of the AD-genome allopolyploids.
Long-distance dispersal played a role not only in diversification of major
evolutionary lines but also in speciation within Gossypium genome groups.
Examples include dispersals from southern Mexico to Peru (G. raimondii),
from northern Mexico to the Galapagos Islands (G. klotzschianum), from
western South America to the Galapagos Islands (G. darwinii), from Africa to
the Cape Verde Islands (G. capitis-viridis), and from the neotropics to the
Hawaiian Islands (G. tomentosum).
6 Seed and Fiber Diversity and Seed Dispersal
An additional perspective offered by the phylogeny of the genus (Fig. 1) con-
cerns the evolutionary history of seeds and their associated single-celled epi-
dermal trichomes, known as hairs in the wild species and lint and fuzz fibers
in the cultivated taxa. The seeds and their coverings are extraordinarily
Evolution and Natural History of the Cotton Genus 13
diverse in Gossypium, as shown in Fig. 2, which shows a sampling of the
different lineages of wild species and two cultivated species (G. arboreum and
G. hirsutum) for comparison. Both wild and cultivated cottons produce fiber
on the seed coat, but there are striking morphological and structural differ-
ences between these fibers, the most obvious of which is their size. Some D-
genome species (G. thurberi, G. trilobum, G. davidsonii, and G. klotzschianum)
do not possess obvious seed hairs, but they actually are present as develop-
mentally repressed structures not visible to the unaided eye (Applequist,
Cronn and Wendel 2001). Similarly, the three D-genome species of subsec-
tion Cauducibracteolata give the appearance of being hairless but, in fact,
Fig. 2 Representative seed and trichome diversity in Gossypium. Seed and trichome size and
morphology are exceedingly variable in the genus. Most wild species have relatively small
seeds (<5mm in any dimension) with equally short fibers. Long (spinnable) fiber evolved only
once, in the ancestor of modern A-genome cottons, which subsequently donated this capacity
to modern tetraploid species, including the commercially important G. hirsutum and G.
barbadense, at the time of allopolyploid formation in the mid-Pleistocene. See text for addi-
tional detail. Key to species: Cult. AD1 ¼ G. hirsutum TM1; Wild AD1 ¼ G. hirsutum Tx2094
from theYucatanPeninsula;AD3¼G. tomentosumWT936 fromHawaii; C1¼G. sturtianumC1-
4 from Australia; Cult. A2¼ G. arboreumAKA8401; Wild A1¼ G. herbaceum subsp. africanum
from Botswana; D5 ¼ G. raimondii from Peru; D3 ¼ G. davidsoniiD3d-32 from Baja California;
F1 ¼ G. longicalyx F1-3 from Tanzania; B1 ¼ G. anomalum B1-1 from Africa (See Color Insert)
14 J.F. Wendel et al.
have seed hairs that are tightly appressed to the seed. Cultivated lint fiber is a
single cell of almost pure cellulose, which elongates during development,
depending on the species, to a final length of two to six centimeters (Kim
and Triplett 2001). The wild-type fiber cell is composed mostly of cellulose
and suberin, and elongates to less than one centimeter (Ryser and Holloway
1985; Applequist, Cronn and Wendel 2001). These and many other differ-
ences (Fryxell 1979; Hutchinson and Stephens 1945) reflect both natural
evolutionary processes as well as human-mediated selection during domes-tication. The duration of the elongation phase and the timing of onset of
secondary wall synthesis appear to be key determinants of the final length of
the fiber in both wild and cultivated plants (Applequist, Cronn, and Wendel,
2001). Phylogenetic analysis of growth rates has shown that the evolutionary
innovation of prolonged elongation arose in the F-genome/A-genome line-
age, which may have facilitated the original domestication of the A-genome
cottons. This trait of prolonged elongation was passed on to the allopoly-
ploids, which in turn was a key component of their eventual domestica-
tion (Applequist, Cronn, and Wendel 2001). Relatively little is known
about the developmental and genetic underpinnings of the diverse morphol-
ogies illustrated in Fig. 2, but an improved understanding of the changes that
occurred during evolution and domestication may have implications for crop
improvement.
In nature, seed dispersal inGossypium often follows a ‘‘shaker’’ model, where
erect, mature capsules dehisce along the sutures and the seeds are distributed
near the parental plant as wind shakes the branches. This likely is the ancestral
method of seed dispersal in the genus, as it occurs in all species of the B-, C-, E-,
F-, and D- (in part) genome groups and in one species (G. bickii) of the G-
genome group. The A-, AD-, some D-genome species, and G- and K-genome
species have evolved other mechanisms of seed dispersal, with perhaps the most
noteworthy innovation being the fat bodies to facilitate ant dispersal on the
seeds of the K-genome species (Seelanan, Brubaker, Stewart, Craven and
Wendel 1999). The development of spinnable fibers apparently has occurred
only once in the history of Gossypium, in the ancestor of the two A-genome
species which became the progenitor of the A-subgenome of the tetraploids.
The evolutionary ‘‘purpose’’ of epidermal seed hairs, or trichomes, is amatter
of speculation. Fryxell (1979) suggested that elongated fibers aid dispersal
by birds, an hypothesis that gains credibility by observations by one of us
(J. Stewart) of a bird’s nest in NW Puerto Rico that contained numerous seeds
of feral G. hirsutum, as well as a collection of G. darwinii from a finch’s nest in
the Galapagos Islands (JFW, unpubl.). One might also speculate that fibers
serve to inhibit germination unless there is sufficient moisture to saturate the
fibers; should germination occur following a light rain, there might not be
sufficient water for subsequent survival of the seedling. In this respect the waxy
coating of the fibers would repel water, to a point, and thus prevent premature
germination. A related possibility is that seed hairs function as ‘‘biological
incubators’’ to facilitate germination only when ecological conditions are
Evolution and Natural History of the Cotton Genus 15
appropriate, by recruiting particular microbial communities under appropriate
moisture regimes. Finally, two G-genome species (G. australe, G. nelsonii) have
evolved stiff straight seed hairs that facilitate wind dispersal in that the stiffening
hairs function to extrude seeds from the locules of the dehisced capsule.
7 Genetic Diversity in the Cultivated Cottons
Domestication has altered the genetic composition of the four cultivated species
in comparison to their wild relatives. As is typical of most wild Gossypium
species, the pre-domesticated cotton species probably had restricted distribu-
tions (Brubaker, Bourland and Wendel 1999), although we cannot be certain
of this because post-domestication, human-mediated germplasm diffusion has
partially (G. barbadense and G. hirsutum) or completely (G. herbaceum and
G. arboreum) obscured the geographic and genetic origins of each species. It
is clear, however, that the indigenous ranges of the four cotton species exp-
anded considerably as cultigens. Eventually this brought G. barbadense and
G. hirsutum into sympatry in the New World, and in the Old World the ranges
of G. herbaceum and G. arboreum also intersected. The consequence was inter-
specific gene flow prior to the initiation of deliberate bi-specific breeding
programs (e.g., the Acala and Pima cultivar families). Among indigenous New
World cotton populations, natural introgression patterns appear to be biased
toward the transfer of G. barbadense alleles into G. hirsutum, particularly in the
Caribbean where the ranges of the two species overlap to the greatest extent
(Wendel, Brubaker and Percival 1992; Brubaker and Wendel 1994; Brubaker,
Koontz and Wendel 1993; Percy and Wendel 1990). Among the modern elite
cultivars, however, the converse is more prevalent. Estimates based on RFLP
data suggest that up to 8.9% of alleles in modern G. barbadense cultivars may
have originated from G. hirsutum (Wang, Dong and Paterson 1995). The Old
World cotton species co-occur in India, northern Africa and China, and there is
evidence for low levels of interspecific gene flow, which may explain in part the
considerable morphological overlap between the two species (Wendel, Olsen and
Stewart 1989).
While pre- and post- domestication interspecific gene flowmay havemingled
the genetic composition of cotton species to some extent, the genetic winnow-
ing that accompanied human selection progressively narrowed the total avail-
able genetic diversity. In the earliest stages of domestication, appreciable
levels of genetic diversity were captured among geographic foci of agronomic
development, often recognized as ‘‘races’’ (Hutchinson 1951; Hutchinson
1954; Hutchinson and Ghose, 1937; Hutchinson 1962; reviewed by Brubaker,
Bourland andWendel 1999), but the modern elite cultivars now contain only a
fraction of this original diversity. As facultative self-pollinators, cotton spe-
cies tolerate inbreeding, and the most recent stages of domestication acceler-
ated the progressive purge of alleles, resulting in modern elite cultivars with
reduced levels of genetic diversity.
16 J.F. Wendel et al.
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Evolution and Natural History of the Cotton Genus 17
Despite the ready availability of molecular markers over the past ten years,
the most informative set of comparative data regarding genetic diversity of
Gossypium species can be found in a series of early isozyme studies (Table 2).
The numbers indicate that the wild tetraploid species have levels of genetic
diversity consistent with their occurrence as island endemics (G. darwinii and
G. tomentosum) or their rarity (G.mustelinum). To the extent that the progenitorpopulations of the cotton species were similarly restricted in distribution, they
might have been similarly depauperate genetically. The cotton species as they
currently exist, however, contain appreciable albeit unremarkable levels of
genetic diversity relative to plants in general (Table 2). Of the four cotton
species, G. hirsutum contains the highest levels of genetic diversity, and it is
here that the genetic consequences of domestication are most evident, as the
modern upland cultivars contain only half of the genetic diversity available.
Gossypium barbadense cultivars, having undergone less intensive selection, retain
a greater proportion of the diversity present in the species as a whole.More recent
molecular marker studies (using RFLPs, RAPDs, AFLPs, or SSRs), while not
directly comparable andwhile focused onG. hirsutum, have validated these initial
genetic ‘‘portraits’’ (Abdalla, Reddy, El-Zik and Pepper 2001; Brubaker and
Wendel 1994; Hawkins, Pleasants and Wendel 2005; Iqbal Reddy, El-Zik and
Pepper 2001; Khan, Hussain, Askari, Stewart, Malik and Zafar 2000; Lacape,
Dessauw,Rajab,Noyer andHau 2007; Liu, Cantrell,McCarty and Stewart 2000;
Liu, Guo, Lin, Nie and Zhang 2005; Pillay and Myers 1999; Rungis, Llewellyn,
Dennis and Lyon 2005), with paucity of genetic diversity among the modern
Upland cultivars as a recurring theme (Lacape,Dessauw,Rajab,Noyer, andHau
2007). One practical consequence of this, exacerbated by the presence of a
genome that contains 26 chromosomes, is that marker-assisted selection in
Upland cotton breeding is less advanced than it is for other crops. Accordingly,
geneticists continue to exploit the more accessible interspecific genetic differ-
ences between G. barbadense and G. hirsutum and between G. arboreum and
G. herbaceum (Ulloa, Brubaker and Chee 2007).
8 Diversity and Crop Improvement
One of the opportunities that arises from an appreciation of the evolutionary
history and diversity of Gossypium is that of deliberate introgression of useful
genes from various wild sources of germplasm. It is a truism that the morpho-
logical and ecological breadth encompassed by the wild species must have
parallels in the underlying genes that control, for example, physiology, chem-
istry, disease resistance traits, and fiber characteristics. The wild species of
cotton, consequently, represent an ample genetic repository for potential
exploitation by cotton breeders. Although these wild species remain a largely
untapped genetic resource, there are many examples of their inclusion in breed-
ing programs (reviewed by McCarty and Percy 2001). Cotton improvement
18 J.F. Wendel et al.
programs have exploited diploid species for genes for fiber strength, disease
resistance, cytoplasmic male sterility and fertility restoration, whereas genes
for disease resistance, nectariless, and glandless cotton have been deliberately
introduced from wild and feral tetraploids. These genetic enhancements,
involving intentional interspecific introgression from a minimum of two allo-
polyploid and four diploid Gossypium species (Meredith 1991; Meyer 1974;
Narayanan, Singh and Varma 1984; Niles and Feaster 1984), were obtained
through classical genetic and plant breeding approaches. Further exploitation
of wild Gossypium and more phylogenetically distant sources of germplasm will
employ these traditional methods as well as genetic engineering (Stewart 1995).
This promise is being realized, as efficient transformation systems have been
developed (see Chapter 8 by Trolinder, this volume). Herbicide tolerant, insect
resistant, and fiber-modified transgenic cultivars are now widespread, account-
ing for the majority of cotton grown in the world today (see Chapter 19 by
Davis, this volume).
Acknowledgments We are grateful to C. Grover and G. Courtney for help with the figures
and to the funding agencies that supported much of the work synthesized here. This includes
the National Science Foundation and the USDA in the US, and CSIRO in Australia.
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22 J.F. Wendel et al.
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https://www.researchgate.net/publication/226492080
	Evolution and Natural History of the Cotton Genus
	1 Introduction to Gossypium diversity
	2 Origin of the Genus Gossypium
	3 Diversification and Speciation of the Diploid Cotton Species
	3.1 Australian Species
	3.2 African-Asian Species
	3.3 American Diploid Species
	4 Origin and Diversification of the Polyploid Cottons
	5 Phylogenetic Relationships in the Genus
	6 Seed and Fiber Diversity and Seed Dispersal
	7 Genetic Diversity in the Cultivated Cottons
	8 Diversity and Crop Improvement
	References